Regulation of Metabolic Processes by Hydrogen Peroxide Generated by NADPH Oxidases
Abstract
:1. Introduction
2. NOX Family
2.1. Hydrogen Peroxide Production
2.2. Tissue Distribution of NOX Proteins
2.3. Structure and Regulation of NOX
2.4. The Role of NOXs in Human Physiology and Pathophysiology
2.5. Effect of NOX-Derived H2O2 on the Tissues
2.5.1. Liver
2.5.2. Adipose Tissue and Other Tissues
3. Conclusions
Funding
Conflicts of Interest
References
- He, L.; He, T.; Farrar, S.; Ji, L.; Liu, T.; Ma, X. Antioxidants maintain cellular redox homeostasis by elimination of reactive oxygen species. Cell Physiol. Biochem. 2017, 44, 532–553. [Google Scholar] [CrossRef] [PubMed]
- Snezhkina, A.V.; Kudryavtseva, A.V.; Kardymon, O.L.; Savvateeva, M.V.; Melnikova, N.V.; Krasnov, G.S.; Dmitriev, A.A. ROS generation and antioxidant defense systems in normal and malignant cells. Oxid. Med. Cell Longev. 2019, 2019, 6175804. [Google Scholar] [CrossRef] [PubMed]
- Ighodaro, O.M.; Akinloye, O.A. First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defence grid. Alexandria J. Med. 2018, 54, 287–293. [Google Scholar] [CrossRef] [Green Version]
- Yang, S.; Lian, G. ROS and diseases: Role in metabolism and energy supply. Mol. Cell Biochem. 2020, 467, 1–12. [Google Scholar] [CrossRef] [PubMed]
- Osorio Alves, J.; Matta Pereira, L.; Cabral Coutinho do Rego Monteiro, I.; Pontes Dos Santos, L.H.; Soares Marreiros Ferraz, A.; Carneiro Loureiro, A.C.; Calado Lima, C.; Leal-Cardoso, J.H.; Pires Carvalho, D.; Soares Fortunato, R.; et al. Strenuous acute exercise induces slow and fast twitch-dependent NADPH oxidase expression in rat skeletal muscle. Antioxidants (Basel) 2020, 9, 57. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sakellariou, G.K.; Vasilaki, A.; Palomero, J.; Kayani, A.; Zibrik, L.; McArdle, A.; Jackson, M.J. Studies of mitochondrial and nonmitochondrial sources implicate nicotinamide adenine dinucleotide phosphate oxidase(s) in the increased skeletal muscle superoxide generation that occurs during contractile activity. Antioxid. Redox Signal. 2013, 18, 603–621. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Breton-Romero, R.; Lamas, S. Hydrogen peroxide signaling in vascular endothelial cells. Redox Biol. 2014, 2, 529–534. [Google Scholar] [CrossRef] [Green Version]
- Sundaresan, M.; Yu, Z.X.; Ferrans, V.J.; Sulciner, D.J.; Gutkind, J.S.; Irani, K.; Goldschmidt-Clermont, P.J.; Finkel, T. Regulation of reactive-oxygen-species generation in fibroblasts by Rac1. Biochem. J. 1996, 318 Pt 2, 379–382. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bedard, K.; Krause, K.H. The NOX family of ROS-generating NADPH oxidases: Physiology and pathophysiology. Physiol. Rev. 2007, 87, 245–313. [Google Scholar] [CrossRef] [PubMed]
- Hajjar, C.; Cherrier, M.V.; Dias Mirandela, G.; Petit-Hartlein, I.; Stasia, M.J.; Fontecilla-Camps, J.C.; Fieschi, F.; Dupuy, J. The NOX family of proteins is also present in bacteria. mBio 2017, 8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Babior, B.M.; Lambeth, J.D.; Nauseef, W. The neutrophil NADPH oxidase. Arch. Biochem. Biophys. 2002, 397, 342–344. [Google Scholar] [CrossRef]
- Burdon, R.H. Superoxide and hydrogen peroxide in relation to mammalian cell proliferation. Free Radic. Biol. Med. 1995, 18, 775–794. [Google Scholar] [CrossRef]
- Lambeth, J.D.; Cheng, G.; Arnold, R.S.; Edens, W.A. Novel homologs of gp91phox. Trends Biochem. Sci. 2000, 25, 459–461. [Google Scholar] [CrossRef]
- Sumimoto, H. Structure, regulation and evolution of Nox-family NADPH oxidases that produce reactive oxygen species. FEBS J. 2008, 275, 3249–3277. [Google Scholar] [CrossRef]
- Magnani, F.; Nenci, S.; Millana Fananas, E.; Ceccon, M.; Romero, E.; Fraaije, M.W.; Mattevi, A. Crystal structures and atomic model of NADPH oxidase. Proc. Natl. Acad. Sci. USA 2017, 114, 6764–6769. [Google Scholar] [CrossRef] [Green Version]
- Pryor, W.A. Oxy-radicals and related species: Their formation, lifetimes, and reactions. Annu. Rev. Physiol. 1986, 48, 657–667. [Google Scholar] [CrossRef] [PubMed]
- Ferrer-Sueta, G.; Radi, R. Chemical biology of peroxynitrite: Kinetics, diffusion, and radicals. ACS Chem. Biol. 2009, 4, 161–177. [Google Scholar] [CrossRef]
- Bienert, G.P.; Chaumont, F. Aquaporin-facilitated transmembrane diffusion of hydrogen peroxide. Biochim. Biophys. Acta 2014, 1840, 1596–1604. [Google Scholar] [CrossRef]
- Rhee, S.G.; Bae, Y.S.; Lee, S.R.; Kwon, J. Hydrogen peroxide: A key messenger that modulates protein phosphorylation through cysteine oxidation. Sci. STKE 2000, 2000, pe1. [Google Scholar] [CrossRef]
- Krause, K.H. Tissue distribution and putative physiological function of NOX family NADPH oxidases. Jpn. J. Infect. Dis. 2004, 57, S28–S29. [Google Scholar]
- Bedard, K.; Lardy, B.; Krause, K.H. NOX family NADPH oxidases: Not just in mammals. Biochimie 2007, 89, 1107–1112. [Google Scholar] [CrossRef] [PubMed]
- Buvelot, H.; Jaquet, V.; Krause, K.H. Mammalian NADPH oxidases. Methods Mol. Biol. 2019, 1982, 17–36. [Google Scholar] [PubMed]
- Katsuyama, M.; Matsuno, K.; Yabe-Nishimura, C. Physiological roles of NOX/NADPH oxidase, the superoxide-generating enzyme. J. Clin. Biochem. Nutr. 2012, 50, 9–22. [Google Scholar] [CrossRef] [Green Version]
- Brown, D.I.; Griendling, K.K. Nox proteins in signal transduction. Free Radic. Biol. Med. 2009, 47, 1239–1253. [Google Scholar] [CrossRef] [Green Version]
- Al Ghouleh, I.; Khoo, N.K.; Knaus, U.G.; Griendling, K.K.; Touyz, R.M.; Thannickal, V.J.; Barchowsky, A.; Nauseef, W.M.; Kelley, E.E.; Bauer, P.M.; et al. Oxidases and peroxidases in cardiovascular and lung disease: New concepts in reactive oxygen species signaling. Free Radic. Biol. Med. 2011, 51, 1271–1288. [Google Scholar] [CrossRef] [Green Version]
- Ambasta, R.K.; Kumar, P.; Griendling, K.K.; Schmidt, H.H.; Busse, R.; Brandes, R.P. Direct interaction of the novel Nox proteins with p22phox is required for the formation of a functionally active NADPH oxidase. J. Biol. Chem. 2004, 279, 45935–45941. [Google Scholar] [CrossRef] [Green Version]
- Groemping, Y.; Lapouge, K.; Smerdon, S.J.; Rittinger, K. Molecular basis of phosphorylation-induced activation of the NADPH oxidase. Cell 2003, 113, 343–355. [Google Scholar] [CrossRef]
- Hiroaki, H.; Ago, T.; Ito, T.; Sumimoto, H.; Kohda, D. Solution structure of the PX domain, a target of the SH3 domain. Nat. Struct. Biol. 2001, 8, 526–530. [Google Scholar] [CrossRef]
- Bokoch, G.M. Regulation of innate immunity by Rho GTPases. Trends Cell Biol. 2005, 15, 163–171. [Google Scholar] [CrossRef]
- Mizuno, T.; Kaibuchi, K.; Ando, S.; Musha, T.; Hiraoka, K.; Takaishi, K.; Asada, M.; Nunoi, H.; Matsuda, I.; Takai, Y. Regulation of the superoxide-generating NADPH oxidase by a small GTP-binding protein and its stimulatory and inhibitory GDP/GTP exchange proteins. J. Biol. Chem. 1992, 267, 10215–10218. [Google Scholar]
- Han, C.H.; Freeman, J.L.; Lee, T.; Motalebi, S.A.; Lambeth, J.D. Regulation of the neutrophil respiratory burst oxidase. Identification of an activation domain in p67(phox). J. Biol. Chem. 1998, 273, 16663–16668. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Diebold, B.A.; Bokoch, G.M. Molecular basis for Rac2 regulation of phagocyte NADPH oxidase. Nat. Immunol. 2001, 2, 211–215. [Google Scholar] [CrossRef]
- Lapouge, K.; Smith, S.J.; Walker, P.A.; Gamblin, S.J.; Smerdon, S.J.; Rittinger, K. Structure of the TPR domain of p67phox in complex with Rac.GTP. Mol. Cell 2000, 6, 899–907. [Google Scholar] [CrossRef]
- Geiszt, M.; Lekstrom, K.; Witta, J.; Leto, T.L. Proteins homologous to p47phox and p67phox support superoxide production by NAD(P)H oxidase 1 in colon epithelial cells. J. Biol. Chem. 2003, 278, 20006–20012. [Google Scholar] [CrossRef] [Green Version]
- Ueno, N.; Takeya, R.; Miyano, K.; Kikuchi, H.; Sumimoto, H. The NADPH oxidase Nox3 constitutively produces superoxide in a p22phox-dependent manner: Its regulation by oxidase organizers and activators. J. Biol. Chem. 2005, 280, 23328–23339. [Google Scholar] [CrossRef] [Green Version]
- Ueyama, T.; Geiszt, M.; Leto, T.L. Involvement of Rac1 in activation of multicomponent Nox1- and Nox3-based NADPH oxidases. Mol. Cell Biol. 2006, 26, 2160–2174. [Google Scholar] [CrossRef] [Green Version]
- Martyn, K.D.; Frederick, L.M.; von Loehneysen, K.; Dinauer, M.C.; Knaus, U.G. Functional analysis of Nox4 reveals unique characteristics compared to other NADPH oxidases. Cell Signal. 2006, 18, 69–82. [Google Scholar] [CrossRef]
- Lyle, A.N.; Deshpande, N.N.; Taniyama, Y.; Seidel-Rogol, B.; Pounkova, L.; Du, P.; Papaharalambus, C.; Lassegue, B.; Griendling, K.K. Poldip2, a novel regulator of Nox4 and cytoskeletal integrity in vascular smooth muscle cells. Circ. Res. 2009, 105, 249–259. [Google Scholar] [CrossRef] [Green Version]
- Banfi, B.; Molnar, G.; Maturana, A.; Steger, K.; Hegedus, B.; Demaurex, N.; Krause, K.H. A Ca(2+)-activated NADPH oxidase in testis, spleen, and lymph nodes. J. Biol. Chem. 2001, 276, 37594–37601. [Google Scholar] [CrossRef] [Green Version]
- Cheng, G.; Cao, Z.; Xu, X.; van Meir, E.G.; Lambeth, J.D. Homologs of gp91phox: Cloning and tissue expression of Nox3, Nox4, and Nox5. Gene 2001, 269, 131–140. [Google Scholar] [CrossRef]
- Banfi, B.; Tirone, F.; Durussel, I.; Knisz, J.; Moskwa, P.; Molnar, G.Z.; Krause, K.H.; Cox, J.A. Mechanism of Ca2+ activation of the NADPH oxidase 5 (NOX5). J. Biol. Chem. 2004, 279, 18583–18591. [Google Scholar] [CrossRef] [Green Version]
- Chen, F.; Pandey, D.; Chadli, A.; Catravas, J.D.; Chen, T.; Fulton, D.J. Hsp90 regulates NADPH oxidase activity and is necessary for superoxide but not hydrogen peroxide production. Antioxid. Redox Signal 2011, 14, 2107–2119. [Google Scholar] [CrossRef] [Green Version]
- Fu, X.; Beer, D.G.; Behar, J.; Wands, J.; Lambeth, D.; Cao, W. cAMP-response element-binding protein mediates acid-induced NADPH oxidase NOX5-S expression in Barrett esophageal adenocarcinoma cells. J. Biol. Chem. 2006, 281, 20368–20382. [Google Scholar] [CrossRef] [Green Version]
- Dupuy, C.; Ohayon, R.; Valent, A.; Noel-Hudson, M.S.; Deme, D.; Virion, A. Purification of a novel flavoprotein involved in the thyroid NADPH oxidase. Cloning of the porcine and human cdnas. J. Biol. Chem. 1999, 274, 37265–37269. [Google Scholar] [CrossRef] [Green Version]
- De Deken, X.; Wang, D.; Dumont, J.E.; Miot, F. Characterization of ThOX proteins as components of the thyroid H(2)O(2)-generating system. Exp. Cell Res. 2002, 273, 187–196. [Google Scholar] [CrossRef] [PubMed]
- Sugawara, M.; Sugawara, Y.; Wen, K.; Giulivi, C. Generation of oxygen free radicals in thyroid cells and inhibition of thyroid peroxidase. Exp. Biol Med. (Maywood) 2002, 227, 141–146. [Google Scholar] [CrossRef]
- Ameziane-El-Hassani, R.; Morand, S.; Boucher, J.L.; Frapart, Y.M.; Apostolou, D.; Agnandji, D.; Gnidehou, S.; Ohayon, R.; Noel-Hudson, M.S.; Francon, J.; et al. Dual oxidase-2 has an intrinsic Ca2+-dependent H2O2-generating activity. J. Biol. Chem. 2005, 280, 30046–30054. [Google Scholar] [CrossRef] [Green Version]
- Kishida, K.T.; Hoeffer, C.A.; Hu, D.; Pao, M.; Holland, S.M.; Klann, E. Synaptic plasticity deficits and mild memory impairments in mouse models of chronic granulomatous disease. Mol. Cell Biol. 2006, 26, 5908–5920. [Google Scholar] [CrossRef] [Green Version]
- Panday, A.; Sahoo, M.K.; Osorio, D.; Batra, S. NADPH oxidases: An overview from structure to innate immunity-associated pathologies. Cell Mol. Immunol. 2015, 12, 5–23. [Google Scholar] [CrossRef] [Green Version]
- Sorce, S.; Krause, K.H. NOX enzymes in the central nervous system: From signaling to disease. Antioxid. Redox Signal. 2009, 11, 2481–2504. [Google Scholar] [CrossRef]
- Arimura, Y.; Goto, A.; Yamashita, K.; Endo, T.; Ikeda, H.; Tanaka, K.; Tsutsumi, H.; Shinomura, Y.; Imai, K. Intractable colitis associated with chronic granulomatous disease. J. Med. Microbiol. 2006, 55, 1587–1590. [Google Scholar] [CrossRef] [Green Version]
- Haque, M.Z.; Majid, D.S. Assessment of renal functional phenotype in mice lacking gp91PHOX subunit of NAD(P)H oxidase. Hypertension 2004, 43, 335–340. [Google Scholar] [CrossRef] [Green Version]
- Henriquez-Olguin, C.; Knudsen, J.R.; Raun, S.H.; Li, Z.; Dalbram, E.; Treebak, J.T.; Sylow, L.; Holmdahl, R.; Richter, E.A.; Jaimovich, E.; et al. Cytosolic ROS production by NADPH oxidase 2 regulates muscle glucose uptake during exercise. Nat. Commun. 2019, 10, 4623. [Google Scholar] [CrossRef] [Green Version]
- Dikalova, A.; Clempus, R.; Lassegue, B.; Cheng, G.; McCoy, J.; Dikalov, S.; San Martin, A.; Lyle, A.; Weber, D.S.; Weiss, D.; et al. Nox1 overexpression potentiates angiotensin II-induced hypertension and vascular smooth muscle hypertrophy in transgenic mice. Circulation 2005, 112, 2668–2676. [Google Scholar] [CrossRef] [Green Version]
- Fukui, T.; Ishizaka, N.; Rajagopalan, S.; Laursen, J.B.; Capers, Q.t.; Taylor, W.R.; Harrison, D.G.; de Leon, H.; Wilcox, J.N.; Griendling, K.K. p22phox mRNA expression and NADPH oxidase activity are increased in aortas from hypertensive rats. Circ. Res. 1997, 80, 45–51. [Google Scholar] [CrossRef]
- Rokutan, K.; Kawahara, T.; Kuwano, Y.; Tominaga, K.; Nishida, K.; Teshima-Kondo, S. Nox enzymes and oxidative stress in the immunopathology of the gastrointestinal tract. Semin. Immunopathol. 2008, 30, 315–327. [Google Scholar] [CrossRef]
- Paffenholz, R.; Bergstrom, R.A.; Pasutto, F.; Wabnitz, P.; Munroe, R.J.; Jagla, W.; Heinzmann, U.; Marquardt, A.; Bareiss, A.; Laufs, J.; et al. Vestibular defects in head-tilt mice result from mutations in Nox3, encoding an NADPH oxidase. Genes Dev. 2004, 18, 486–491. [Google Scholar] [CrossRef] [Green Version]
- Accetta, R.; Damiano, S.; Morano, A.; Mondola, P.; Paterno, R.; Avvedimento, E.V.; Santillo, M. Reactive oxygen species derived from NOX3 and NOX5 drive differentiation of human oligodendrocytes. Front. Cell Neurosci. 2016, 10, 146. [Google Scholar] [CrossRef] [Green Version]
- Schroder, K.; Wandzioch, K.; Helmcke, I.; Brandes, R.P. Nox4 acts as a switch between differentiation and proliferation in preadipocytes. Arterioscler. Thromb. Vasc. Biol. 2009, 29, 239–245. [Google Scholar] [CrossRef] [Green Version]
- Mahadev, K.; Motoshima, H.; Wu, X.; Ruddy, J.M.; Arnold, R.S.; Cheng, G.; Lambeth, J.D.; Goldstein, B.J. The NAD(P)H oxidase homolog Nox4 modulates insulin-stimulated generation of H2O2 and plays an integral role in insulin signal transduction. Mol. Cell Biol. 2004, 24, 1844–1854. [Google Scholar] [CrossRef] [Green Version]
- Plecita-Hlavata, L.; Jaburek, M.; Holendova, B.; Tauber, J.; Pavluch, V.; Berkova, Z.; Cahova, M.; Schroder, K.; Brandes, R.P.; Siemen, D.; et al. Glucose-stimulated insulin secretion fundamentally requires H2O2 signaling by NADPH Oxidase 4. Diabetes 2020, 69, 1341–1354. [Google Scholar] [CrossRef]
- Drummond, G.R.; Sobey, C.G. Endothelial NADPH oxidases: Which NOX to target in vascular disease? Trends Endocrinol. Metab. 2014, 25, 452–463. [Google Scholar] [CrossRef]
- Guo, S.; Chen, X. The human Nox4: Gene, structure, physiological function and pathological significance. J. Drug Target. 2015, 23, 888–896. [Google Scholar] [CrossRef] [PubMed]
- Gray, S.P.; Di Marco, E.; Kennedy, K.; Chew, P.; Okabe, J.; El-Osta, A.; Calkin, A.C.; Biessen, E.A.; Touyz, R.M.; Cooper, M.E.; et al. Reactive oxygen species can provide atheroprotection via NOX4-dependent inhibition of inflammation and vascular remodeling. Arterioscler. Thromb. Vasc. Biol. 2016, 36, 295–307. [Google Scholar] [CrossRef] [Green Version]
- Ghanbari, H.; Keshtgar, S.; Kazeroni, M. Inhibition of the CatSper channel and NOX5 enzyme activity affects the functions of the progesterone-stimulated human sperm. Iran. J. Med. Sci. 2018, 43, 18–25. [Google Scholar]
- Montezano, A.C.; De Lucca Camargo, L.; Persson, P.; Rios, F.J.; Harvey, A.P.; Anagnostopoulou, A.; Palacios, R.; Gandara, A.C.P.; Alves-Lopes, R.; Neves, K.B.; et al. NADPH Oxidase 5 is a pro-contractile nox isoform and a point of cross-talk for calcium and redox signaling-implications in vascular function. J. Am. Heart Assoc. 2018, 7. [Google Scholar] [CrossRef] [Green Version]
- Moreno, J.C.; Bikker, H.; Kempers, M.J.; van Trotsenburg, A.S.; Baas, F.; de Vijlder, J.J.; Vulsma, T.; Ris-Stalpers, C. Inactivating mutations in the gene for thyroid oxidase 2 (THOX2) and congenital hypothyroidism. N. Engl. J. Med. 2002, 347, 95–102. [Google Scholar] [CrossRef] [Green Version]
- Knaus, U.G. Oxidants in physiological processes. Handb. Exp. Pharmacol. 2020. [CrossRef]
- Liu, E.; Perl, A. Pathogenesis and treatment of autoimmune rheumatic diseases. Curr. Opin. Rheumatol. 2019, 31, 307–315. [Google Scholar] [CrossRef]
- Laddha, A.P.; Kulkarni, Y.A. NADPH oxidase: A membrane-bound enzyme and its inhibitors in diabetic complications. Eur. J. Pharmacol. 2020, 881, 173206. [Google Scholar] [CrossRef] [PubMed]
- Block, M.L. NADPH oxidase as a therapeutic target in Alzheimer’s disease. BMC Neurosci. 2008, 9 (Suppl. 2), S8. [Google Scholar] [CrossRef] [Green Version]
- Wu, D.C.; Teismann, P.; Tieu, K.; Vila, M.; Jackson-Lewis, V.; Ischiropoulos, H.; Przedborski, S. NADPH oxidase mediates oxidative stress in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson’s disease. Proc. Natl. Acad. Sci. USA 2003, 100, 6145–6150. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jiang, J.X.; Torok, N.J. NADPH oxidases in chronic liver diseases. Adv. Hepatol. 2014, 2014. [Google Scholar] [CrossRef] [Green Version]
- Ding, A.; Nathan, C. Analysis of the nonfunctional respiratory burst in murine Kupffer cells. J. Exp. Med. 1988, 167, 1154–1170. [Google Scholar] [CrossRef]
- Mizukami, Y.; Matsubara, F.; Matsukawa, S.; Izumi, R. Cytochemical localization of glutaraldehyde-resistant NAD(P)H-oxidase in rat hepatocytes. Histochemistry 1983, 79, 259–267. [Google Scholar] [CrossRef] [PubMed]
- Jones, S.A.; O’Donnell, V.B.; Wood, J.D.; Broughton, J.P.; Hughes, E.J.; Jones, O.T. Expression of phagocyte NADPH oxidase components in human endothelial cells. Am. J. Physiol. 1996, 271, H1626–H1634. [Google Scholar] [CrossRef]
- Friedman, S.L. Hepatic stellate cells: Protean, multifunctional, and enigmatic cells of the liver. Physiol. Rev. 2008, 88, 125–172. [Google Scholar] [CrossRef]
- Reinehr, R.; Becker, S.; Eberle, A.; Grether-Beck, S.; Haussinger, D. Involvement of NADPH oxidase isoforms and Src family kinases in CD95-dependent hepatocyte apoptosis. J. Biol. Chem. 2005, 280, 27179–27194. [Google Scholar] [CrossRef] [Green Version]
- LaCourse, R.; Ryan, L.; North, R.J. Expression of NADPH oxidase-dependent resistance to listeriosis in mice occurs during the first 6 to 12 h of liver infection. Infect. Immun. 2002, 70, 7179–7181. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Uchikura, K.; Wada, T.; Hoshino, S.; Nagakawa, Y.; Aiko, T.; Bulkley, G.B.; Klein, A.S.; Sun, Z. Lipopolysaccharides induced increases in Fas ligand expression by Kupffer cells via mechanisms dependent on reactive oxygen species. Am. J. Physiol. Gastrointest. Liver Physiol. 2004, 287, G620–G626. [Google Scholar] [CrossRef] [Green Version]
- Rose, M.L.; Rusyn, I.; Bojes, H.K.; Belyea, J.; Cattley, R.C.; Thurman, R.G. Role of Kupffer cells and oxidants in signaling peroxisome proliferator-induced hepatocyte proliferation. Mutat. Res. 2000, 448, 179–192. [Google Scholar] [CrossRef]
- McKim, S.E.; Gabele, E.; Isayama, F.; Lambert, J.C.; Tucker, L.M.; Wheeler, M.D.; Connor, H.D.; Mason, R.P.; Doll, M.A.; Hein, D.W.; et al. Inducible nitric oxide synthase is required in alcohol-induced liver injury: Studies with knockout mice. Gastroenterology 2003, 125, 1834–1844. [Google Scholar] [CrossRef]
- Diaz-Cruz, A.; Guinzberg, R.; Guerra, R.; Vilchis, M.; Carrasco, D.; Garcia-Vazquez, F.J.; Pina, E. Adrenaline stimulates H2O2 generation in liver via NADPH oxidase. Free Radic. Res. 2007, 41, 663–672. [Google Scholar] [CrossRef]
- Diaz-Cruz, A.; Vilchis-Landeros, M.M.; Guinzberg, R.; Villalobos-Molina, R.; Pina, E. NOX2 activated by alpha1-adrenoceptors modulates hepatic metabolic routes stimulated by beta-adrenoceptors. Free Radic. Res. 2011, 45, 1366–1378. [Google Scholar] [CrossRef] [PubMed]
- Vilchis-Landeros, M.; Guinzberg, R.; Riveros-Rosas, H.; Villalobos-Molina, R.; Pina, E. Aquaporin 8 is involved in H2O2-mediated differential regulation of metabolic signaling by alpha1- and beta-adrenoceptors in hepatocytes. FEBS Lett. 2020, 594, 1564–1576. [Google Scholar] [CrossRef]
- Herrera, B.; Murillo, M.M.; Alvarez-Barrientos, A.; Beltran, J.; Fernandez, M.; Fabregat, I. Source of early reactive oxygen species in the apoptosis induced by transforming growth factor-beta in fetal rat hepatocytes. Free Radic. Biol. Med. 2004, 36, 16–26. [Google Scholar] [CrossRef]
- Roma, M.G.; Sanchez Pozzi, E.J. Oxidative stress: A radical way to stop making bile. Ann. Hepatol. 2008, 7, 16–33. [Google Scholar] [CrossRef]
- de Pina, M.Z.; Vazquez-Meza, H.; Pardo, J.P.; Rendon, J.L.; Villalobos-Molina, R.; Riveros-Rosas, H.; Pina, E. Signaling the signal, cyclic AMP-dependent protein kinase inhibition by insulin-formed H2O2 and reactivation by thioredoxin. J. Biol. Chem. 2008, 283, 12373–12386. [Google Scholar] [CrossRef] [Green Version]
- Vazquez-Meza, H.; de Pina, M.Z.; Pardo, J.P.; Riveros-Rosas, H.; Villalobos-Molina, R.; Pina, E. Non-steroidal anti-inflammatory drugs activate NADPH oxidase in adipocytes and raise the H2O2 pool to prevent cAMP-stimulated protein kinase a activation and inhibit lipolysis. BMC Biochem. 2013, 14, 13. [Google Scholar] [CrossRef] [Green Version]
- Becker, S.; Reinehr, R.; Graf, D.; vom Dahl, S.; Haussinger, D. Hydrophobic bile salts induce hepatocyte shrinkage via NADPH oxidase activation. Cell Physiol. Biochem. 2007, 19, 89–98. [Google Scholar] [CrossRef]
- Carmona-Cuenca, I.; Herrera, B.; Ventura, J.J.; Roncero, C.; Fernandez, M.; Fabregat, I. EGF blocks NADPH oxidase activation by TGF-beta in fetal rat hepatocytes, impairing oxidative stress, and cell death. J. Cell Physiol. 2006, 207, 322–330. [Google Scholar] [CrossRef] [PubMed]
- Sancho, P.; Bertran, E.; Caja, L.; Carmona-Cuenca, I.; Murillo, M.M.; Fabregat, I. The inhibition of the epidermal growth factor (EGF) pathway enhances TGF-beta-induced apoptosis in rat hepatoma cells through inducing oxidative stress coincident with a change in the expression pattern of the NADPH oxidases (NOX) isoforms. Biochim. Biophys. Acta 2009, 1793, 253–263. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sancho, P.; Fabregat, I. NADPH oxidase NOX1 controls autocrine growth of liver tumor cells through up-regulation of the epidermal growth factor receptor pathway. J. Biol. Chem. 2010, 285, 24815–24824. [Google Scholar] [CrossRef] [Green Version]
- Guichard, C.; Moreau, R.; Pessayre, D.; Epperson, T.K.; Krause, K.H. NOX family NADPH oxidases in liver and in pancreatic islets: A role in the metabolic syndrome and diabetes? Biochem. Soc. Trans. 2008, 36, 920–929. [Google Scholar] [CrossRef] [Green Version]
- Gao, D.; Nong, S.; Huang, X.; Lu, Y.; Zhao, H.; Lin, Y.; Man, Y.; Wang, S.; Yang, J.; Li, J. The effects of palmitate on hepatic insulin resistance are mediated by NADPH oxidase 3-derived reactive oxygen species through JNK and p38MAPK pathways. J. Biol. Chem. 2010, 285, 29965–29973. [Google Scholar] [CrossRef] [Green Version]
- Rao, M.S.; Reddy, J.K. The relevance of peroxisome proliferation and cell proliferation in peroxisome proliferator-induced hepatocarcinogenesis. Drug Metab. Rev. 1989, 21, 103–110. [Google Scholar]
- Teufelhofer, O.; Parzefall, W.; Kainzbauer, E.; Ferk, F.; Freiler, C.; Knasmuller, S.; Elbling, L.; Thurman, R.; Schulte-Hermann, R. Superoxide generation from Kupffer cells contributes to hepatocarcinogenesis: Studies on NADPH oxidase knockout mice. Carcinogenesis 2005, 26, 319–329. [Google Scholar] [CrossRef] [Green Version]
- Carmiel-Haggai, M.; Cederbaum, A.I.; Nieto, N. A high-fat diet leads to the progression of non-alcoholic fatty liver disease in obese rats. FASEB J. 2005, 19, 136–138. [Google Scholar] [CrossRef]
- Harada, H.; Hines, I.N.; Flores, S.; Gao, B.; McCord, J.; Scheerens, H.; Grisham, M.B. Role of NADPH oxidase-derived superoxide in reduced size liver ischemia and reperfusion injury. Arch. Biochem. Biophys. 2004, 423, 103–108. [Google Scholar] [CrossRef] [PubMed]
- Hines, I.N.; Hoffman, J.M.; Scheerens, H.; Day, B.J.; Harada, H.; Pavlick, K.P.; Bharwani, S.; Wolf, R.; Gao, B.; Flores, S.; et al. Regulation of postischemic liver injury following different durations of ischemia. Am. J. Physiol. Gastrointest. Liver Physiol. 2003, 284, G536–G545. [Google Scholar] [CrossRef] [Green Version]
- Aram, G.; Potter, J.J.; Liu, X.; Wang, L.; Torbenson, M.S.; Mezey, E. Deficiency of nicotinamide adenine dinucleotide phosphate, reduced form oxidase enhances hepatocellular injury but attenuates fibrosis after chronic carbon tetrachloride administration. Hepatology 2009, 49, 911–919. [Google Scholar] [CrossRef] [Green Version]
- Sancho, P.; Mainez, J.; Crosas-Molist, E.; Roncero, C.; Fernandez-Rodriguez, C.M.; Pinedo, F.; Huber, H.; Eferl, R.; Mikulits, W.; Fabregat, I. NADPH oxidase NOX4 mediates stellate cell activation and hepatocyte cell death during liver fibrosis development. PLoS ONE 2012, 7, e45285. [Google Scholar] [CrossRef] [Green Version]
- Bettaieb, A.; Jiang, J.X.; Sasaki, Y.; Chao, T.I.; Kiss, Z.; Chen, X.; Tian, J.; Katsuyama, M.; Yabe-Nishimura, C.; Xi, Y.; et al. Hepatocyte nicotinamide adenine dinucleotide phosphate reduced oxidase 4 regulates stress signaling, fibrosis, and insulin sensitivity during development of steatohepatitis in mice. Gastroenterology 2015, 149, 468–480 e410. [Google Scholar] [CrossRef] [Green Version]
- Jiang, J.X.; Venugopal, S.; Serizawa, N.; Chen, X.; Scott, F.; Li, Y.; Adamson, R.; Devaraj, S.; Shah, V.; Gershwin, M.E.; et al. Reduced nicotinamide adenine dinucleotide phosphate oxidase 2 plays a key role in stellate cell activation and liver fibrogenesis in vivo. Gastroenterology 2010, 139, 1375–1384. [Google Scholar] [CrossRef] [Green Version]
- Lan, T.; Kisseleva, T.; Brenner, D.A. Deficiency of NOX1 or NOX4 prevents liver inflammation and fibrosis in mice through inhibition of hepatic stellate cell activation. PLoS ONE 2015, 10, e0129743. [Google Scholar] [CrossRef] [PubMed]
- Andueza, A.; Garde, N.; Garcia-Garzon, A.; Ansorena, E.; Lopez-Zabalza, M.J.; Iraburu, M.J.; Zalba, G.; Martinez-Irujo, J.J. NADPH oxidase 5 promotes proliferation and fibrosis in human hepatic stellate cells. Free Radic. Biol. Med. 2018, 126, 15–26. [Google Scholar] [CrossRef]
- Holmstrom, K.M.; Finkel, T. Cellular mechanisms and physiological consequences of redox-dependent signalling. Nat. Rev. Mol. Cell Biol. 2014, 15, 411–421. [Google Scholar] [CrossRef]
- Labunskyy, V.M.; Gladyshev, V.N. Role of reactive oxygen species-mediated signaling in aging. Antioxid. Redox Signal. 2013, 19, 1362–1372. [Google Scholar] [CrossRef] [Green Version]
- Finkel, T. Signal transduction by reactive oxygen species. J. Cell Biol. 2011, 194, 7–15. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nelson, K.J.; Bolduc, J.A.; Wu, H.; Collins, J.A.; Burke, E.A.; Reisz, J.A.; Klomsiri, C.; Wood, S.T.; Yammani, R.R.; Poole, L.B.; et al. H2O2 oxidation of cysteine residues in c-Jun N-terminal kinase 2 (JNK2) contributes to redox regulation in human articular chondrocytes. J. Biol. Chem. 2018, 293, 16376–16389. [Google Scholar] [CrossRef] [Green Version]
- Haval, G.A.; Pekhale, K.D.; Perween, N.A.; Ghaskadbi, S.M.; Ghaskadbi, S.S. Excess hydrogen peroxide inhibits head and foot regeneration in hydra by affecting DNA repair and expression of essential genes. J. Biochem. Mol. Toxicol. 2020. [CrossRef]
- Tsubata, T. Involvement of reactive oxygen species (ROS) in BCR signaling as a second messenger. Adv. Exp. Med. Biol. 2020, 1254, 37–46. [Google Scholar]
- Wang, G.; Yang, Q.; Zheng, C.; Li, D.; Li, J.; Zhang, F. Physiological Concentration of H2O2 supports dopamine neuronal survival via activation of Nrf2 signaling in glial cells. Cell Mol. Neurobiol. 2020. [Google Scholar] [CrossRef] [PubMed]
- Rashdan, N.A.; Pattillo, C.B. Hydrogen peroxide in the ER: A tale of triage. Redox Biol. 2020, 28, 101358. [Google Scholar] [CrossRef] [PubMed]
- Bestetti, S.; Galli, M.; Sorrentino, I.; Pinton, P.; Rimessi, A.; Sitia, R.; Medrano-Fernandez, I. Human aquaporin-11 guarantees efficient transport of H2O2 across the endoplasmic reticulum membrane. Redox Biol. 2020, 28, 101326. [Google Scholar] [CrossRef]
- Lismont, C.; Koster, J.; Provost, S.; Baes, M.; Van Veldhoven, P.P.; Waterham, H.R.; Fransen, M. Deciphering the potential involvement of PXMP2 and PEX11B in hydrogen peroxide permeation across the peroxisomal membrane reveals a role for PEX11B in protein sorting. Biochim. Biophys. Acta Biomembr. 2019, 1861, 182991. [Google Scholar] [CrossRef]
- Mukherjee, S.P. Mediation of the antilipolytic and lipogenic effects of insulin in adipocytes by intracellular accumulation of hydrogen peroxide. Biochem. Pharmacol. 1980, 29, 1239–1246. [Google Scholar] [CrossRef]
- Mukherjee, S.P.; Lynn, W.S. Reduced nicotinamide adenine dinucleotide phosphate oxidase in adipocyte plasma membrane and its activation by insulin. Possible role in the hormone’s effects on adenylate cyclase and the hexose monophosphate shunt. Arch. Biochem. Biophys. 1977, 184, 69–76. [Google Scholar] [CrossRef]
- Reth, M. Hydrogen peroxide as second messenger in lymphocyte activation. Nat. Immunol. 2002, 3, 1129–1134. [Google Scholar] [CrossRef]
- Dagnell, M.; Cheng, Q.; Rizvi, S.H.M.; Pace, P.E.; Boivin, B.; Winterbourn, C.C.; Arner, E.S.J. Bicarbonate is essential for protein-tyrosine phosphatase 1B (PTP1B) oxidation and cellular signaling through EGF-triggered phosphorylation cascades. J. Biol. Chem. 2019, 294, 12330–12338. [Google Scholar] [CrossRef] [Green Version]
- Kaul, N.; Gopalakrishna, R.; Gundimeda, U.; Choi, J.; Forman, H.J. Role of protein kinase C in basal and hydrogen peroxide-stimulated NF-kappa B activation in the murine macrophage J774A.1 cell line. Arch. Biochem. Biophys. 1998, 350, 79–86. [Google Scholar] [CrossRef]
- Torres, M.; Forman, H.J. Activation of several MAP kinases upon stimulation of rat alveolar macrophages: Role of the NADPH oxidase. Arch. Biochem. Biophys. 1999, 366, 231–239. [Google Scholar] [CrossRef] [PubMed]
- Brennan, J.P.; Bardswell, S.C.; Burgoyne, J.R.; Fuller, W.; Schroder, E.; Wait, R.; Begum, S.; Kentish, J.C.; Eaton, P. Oxidant-induced activation of type I protein kinase A is mediated by RI subunit interprotein disulfide bond formation. J. Biol. Chem. 2006, 281, 21827–21836. [Google Scholar] [CrossRef] [Green Version]
- Little, S.A.; de Haen, C. Effects of hydrogen peroxide on basal and hormone-stimulated lipolysis in perifused rat fat cells in relation to the mechanism of action of insulin. J. Biol. Chem. 1980, 255, 10888–10895. [Google Scholar]
- Mukherjee, S.P.; Lane, R.H.; Lynn, W.S. Endogenous hydrogen peroxide and peroxidative metabolism in adipocytes in response to insulin and sulfhydryl reagents. Biochem. Pharmacol. 1978, 27, 2589–2594. [Google Scholar] [CrossRef]
- Lawrence, J.C., Jr.; Larner, J. Activation of glycogen synthase in rat adipocytes by insulin and glucose involves increased glucose transport and phosphorylation. J. Biol. Chem. 1978, 253, 2104–2113. [Google Scholar]
- Krieger-Brauer, H.I.; Medda, P.K.; Kather, H. Insulin-induced activation of NADPH-dependent H2O2 generation in human adipocyte plasma membranes is mediated by Galphai2. J. Biol. Chem. 1997, 272, 10135–10143. [Google Scholar] [CrossRef] [Green Version]
- Mahadev, K.; Zilbering, A.; Zhu, L.; Goldstein, B.J. Insulin-stimulated hydrogen peroxide reversibly inhibits protein-tyrosine phosphatase 1b in vivo and enhances the early insulin action cascade. J. Biol. Chem. 2001, 276, 21938–21942. [Google Scholar] [CrossRef] [Green Version]
- Mahadev, K.; Wu, X.; Motoshima, H.; Goldstein, B.J. Integration of multiple downstream signals determines the net effect of insulin on MAP kinase vs. PI 3’-kinase activation: Potential role of insulin-stimulated H(2)O(2). Cell Signal. 2004, 16, 323–331. [Google Scholar] [CrossRef]
- Porras, A.; Zuluaga, S.; Valladares, A.; Alvarez, A.M.; Herrera, B.; Fabregat, I.; Benito, M. Long-term treatment with insulin induces apoptosis in brown adipocytes: Role of oxidative stress. Endocrinology 2003, 144, 5390–5401. [Google Scholar] [CrossRef]
NOX isoforms | High expression | Low to Intermediate Expression | Subcellular Localization |
---|---|---|---|
NOX1 | Colon epithelium | Placenta, uterus prostate, vascular smooth muscle cells, endothelial cells, osteoclasts, retinal pericytes, colon tumor cell lines, Caco-2 DLD-1, and HT-29 | Intracellular membranes close to endoplasmic reticulum, endosomes, and caveolae |
NOX2 | Phagocytic cells | Thymus, small intestine, colon, spleen, pancreas, ovary, placenta, prostate, testis, endothelial cells, smooth muscle, neurons, cardiomyocytes, skeletal muscle myocytes, hepatocytes, and hematopoietic stem cells | Cell membrane and phagosomes |
NOX3 | Inner ear (cochlear, vestibular sensory epithelia, spiral ganglion) | Fetal tissues, skull bone, spleen, kidney, lung, and brain | Plasma membrane |
NOX4 | Kidney (renal distal and proximal tubules) and blood vessels | Placenta, spleen, uterus, pancreas, fetal tissues, adipocytes, fibroblasts, neurons, vascular and endothelial cells, osteoclasts, smooth muscle cells, hematopoietic stem cells, keratinocytes, and melanoma cells | Focal adhesions, endoplasmic reticulum, nucleus, and mitochondrial |
NOX5 | Testis and lymph nodes | Spleen, vascular smooth muscle, bone marrow, pancreas, placenta, ovary, uterus, stomach and fetal tissues | Plasma membrane and endoplasmic reticulum |
DUOX 1 | Thyroid | Airway epithelia, prostate, tongue epithelium, cerebellum, and testis | Plasma membrane |
DUOX 2 | Thyroid | Salivary and rectal glands, gastrointestinal tract (duodenum, colon, cecum), airway epithelia, uterus, gall bladder, pancreatic islets, and prostate | Plasma membrane |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Vilchis-Landeros, M.M.; Matuz-Mares, D.; Vázquez-Meza, H. Regulation of Metabolic Processes by Hydrogen Peroxide Generated by NADPH Oxidases. Processes 2020, 8, 1424. https://doi.org/10.3390/pr8111424
Vilchis-Landeros MM, Matuz-Mares D, Vázquez-Meza H. Regulation of Metabolic Processes by Hydrogen Peroxide Generated by NADPH Oxidases. Processes. 2020; 8(11):1424. https://doi.org/10.3390/pr8111424
Chicago/Turabian StyleVilchis-Landeros, María Magdalena, Deyamira Matuz-Mares, and Héctor Vázquez-Meza. 2020. "Regulation of Metabolic Processes by Hydrogen Peroxide Generated by NADPH Oxidases" Processes 8, no. 11: 1424. https://doi.org/10.3390/pr8111424